Diets of Coastal Bottlenose Dolphins from the U. S. Mid

Home , Atlantic croaker, Cynoscion, Weakfish

MARINE MAMMAL SCIENCE, 20(3):527-545 (July 2004) 0 2004 by the Society for Marine Mammalogy

DIETS OF COASTAL BOTTLENOSE DOLPHINS FROM THE U.S. MID-ATLANTIC COAST DIFFER BY HABITAT DAMONP. GANNON' DANIELLEM. WAPLES Duke University Marine Laboratory, Nicholas School of the Environment and Earth Sciences, Duke University, 135 Duke Marine Lab Road, Beaufort, North Carolina 28516, U.S.A. E-mail: [email protected]

ABSTRACT We recorded 31 species in the stomachs of 146 coastal bottlenose dolphins (Tursiops truncatu) from North Carolina, U.S.A. Sciaenid fishes were the most common prey (frequency of occurrence = 95%). By mass, Atlantic croaker (Micropogonias undulatus) dominated the diet of dolphins that stranded inside estuaries, whereas weakfish (Cynosicon regalis) was most important for dolphins in the ocean. Inshore squid (Loligo sp.) was eaten commonly by dolphins in the ocean, but not by those in the estuaries. There was no significant pattern in prey size associated with dolphin demography, but the proportion of the diet represented by croaker was higher for males than for females, and mature dolphins ate more croaker than did juveniles. Dietary differences between dolphins that stranded in the estuaries and those that stranded on ocean beaches support the hypothesis that some members of the population inhabit the ocean primarily while others reside principally in estuaries. The overwhelming majority of prey were soniferous species (75% of numerical abundance), which is consistent with the hypothesis that bottlenose dolphins use passive listening to locate noise-making fishes. However, spatiotemporal patterns in consumption of Sciaenid fishes did not coincide with their spawning, which is when peak sound production is thought to occur. Key words: coastal bottlenose dolphin, Tursiops trzncatus, food habits, feeding, foraging ecology, Sciaenidae, soniferous fishes, mid-Atlantic, estuary, coastal ocean.

In this paper we quantify the food habits of coastal bottlenose dolphins, Tursiups truncatus, in the waters off the mid-Atlantic coast of the U.S. using traditional stomach content analysis techniques. Previous analyses of bottlenose dolphin food habits in this region were based on small samples, and none investigated differences in feeding habits associated with season, habitat, sex, or age. True (1885) identified common gurnard (Prionutus carolinus) in the stomachs of two dolphins taken by the dolphin fishery in Cape May, New Jersey. Fishermen from Cape Hatteras, North Carolina, told Townsend (1914) that the bottlenose dolphins in that region

Current address: Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236, U.S.A.

527 5 28 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3, 2004 primarily ate seatrout (Cynoscion spp.). Mead and Potter (1990) conducted the most thorough investigation of bottlenose dolphin food habits in the mid-Atlantic region, using a sample of 64 dolphins stranded on the coasts of North Carolina, Virginia, and Maryland. These authors calculated frequencies of prey occurrence and numerical abundance, both of which require large sample sizes, and neither accounts for prey mass (Hyslop 1980). The most important prey found by Mead and Potter (1990) included spot (Leiostomus xantburzls), croaker (Micropogonias undulatus), seatrouts, silver perch (Bairdiella cbtysoura), hake (Uropbycis sp.), and squid (Loligo sp.). We investigated variation in food habits with respect to habitat (coastal ocean us. estuary), season, and demography. In North Carolina bottlenose dolphins move between the ocean and the estuaries.* However, there is evidence from photographic identification and the presence of ectoparasites that some dolphins occupy estuaries primarily, while others stay mainly in the ocean. Some authors hypothesize that pseudostalked barnacles Xenobalanus sp., which attach to the appendages of dolphins, can be used as an indicator of ocean residence (Caldwell and Caldwell 1972, Barros 1993). If some coastal dolphins are primarily oceanic while others are primarily estuarine, one might expect to find differences between the two groups with regard to food habits. We tested the hypothesis that the dolphin diet changes seasonally because many of the species eaten by bottlenose dolphins undergo seasonal migrations. Faced with migrating prey, dolphins can either follow their prey or switch to a different set of prey. Developing the skills to locate and capture prey probably requires an extended period of learning for young bottlenose dolphins. Mann and Smuts (1999) noted that young dolphins begin “play snacking” behavior as early as three weeks of age with objects such as seagrass. Play snacking with fish begins at about week seven. While developing hunting skills, young dolphins may eat prey that are less elusive than those species normally eaten by older dolphins. Smith and Read (1992) found that harbor porpoise (Pbocoena pbocoena) calves eat euphausiids (MeganyctiFbanes norvegica), which are rare in the diets of adult porpoises. Young franciscana (Pontoporia blainvillei) feed on shrimp, whereas adults eat fishes and cephalopods (Rodriguez et al. 2002). Mead and Potter (1990) also concluded that weaning is gradual in bottlenose dolphins, which may reflect the need for young dolphins to augment energy intake from solid food with that of their mother’s milk until they have become proficient at capturing prey. Lactating female mammals typically have the highest energy demands of any demographic group within their species and often have nutrient requirements that differ from other members of their species (e.g., Clutton-Brock et al. 1982, Close et al. 1985, Perez and Mooney 1986). In a comparison of the diets of pregnant and lactating spotted dolphins (Stenella attenuata), Bernard and Hohn (1989) found that lactating spotted dolphins ate more food and increased the proportion of fish relative to squid in their diet. Robertson and Chivers (1997) also found that female spotted dolphins increased their food consumption during lactation. However, Robertson and Chivers (1997) came to the opposite conclusion regarding the relative proportions of squid and fish in the diets of lactating females: lactating females increased the amount of squid in their diet. Cockcroft and Ross (1990) found dietary differences among life history stages of bottlenose dolphins in South Africa. Recently, Kastelein et al. (2002) documented that captive bottlenose dolphins increased their

’ Personal communication from Keith Rittmaster, North Carolina Maratime Museum, 3 15 Front Street., Beaufort, NC 28516, June 2003. GANNON AND WAPLES: BOTTLENOSE DOLPHIN DIET 529 consumption of food little during gestation but that their consumption increased by 58%-97% during lactation.

METHODS We examined the stomach contents of coastal bottlenose dolphins that died of natural causes or that were captured accidentally by commercial fisheries in the estuaries and ocean waters of North Carolina from 1993 to 2001. Two ecotypes of ?: truncatus are recognized on the east coast of the U.S.: a nearshore form known as the “coastal” ecotype and a pelagic form known as the “offshore”ecotype (see Hersh and Duffield 1990; Mead and Potter 1990, 1995; Torres et al. 2003). We restricted our analyses to the coastal form. Offshore dolphins are not thought to come any closer to shore than 7.5 km and coastal dolphins are found from the estuaries out to a distance of 34 km from shore (Torres et al. 2003). We used a hierarchical approach to distinguish between members of the two ecotypes. Dolphin stomachs containing prey known to inhabit only waters greater than 25 m were excluded from analysis (Mead and Potter 1995). The remaining dolphins were categorized on the basis of parasite assemblages. Coastal dolphins were identified by the presence of the trematode Braunina in pyloric and main stomach chambers and offshore dolphins were recognized by the cestodes Pbyllobotbrium and Monorbygma and by the nematode Crassicauda (Mead and Potter 1990, 1995). Categorization of some dolphins was corroborated independently by sighting histories and capture locations. Photo- graphic sighting data of individual dolphins (n = 10) were collected by the contributors to the Mid-Atlantic Bottlenose Dolphin Cata10g.~These ten dolphins were only sighted within 7.5 km of shore and were, therefore, assumed to be of the coastal ecotype. The location of capture was known for seven dolphins; five were captured in pelagic fisheries (>34 km from shore: offshore ecotype) and two were taken in coastal fisheries (c7.5 km from shore: coastal ecotype). The stomach of each dolphin was extracted in its entirety (including esophagus and duodenal ampulla) during necropsies conducted either in the field or in the laboratory. In the lab, the contents of all three stomach chambers were removed for analysis. Intact prey were removed first, then the remaining stomach contents were put in a shallow tray. We topped the tray off with water, gently agitated it, and then decanted floating tissue into a 1-mm sieve. We repeated this process until all floating tissue was separated from the dense bones. We retained the skeletal parts that had sunken to the bottom of the tray and then inspected the contents of the sieve to make sure no hard parts, such as small otoliths, had adhered to the loose flesh that had been poured off. Structures used to identify prey included: sagittal otoliths, dentary bones, and skulls of teleosts; lower mandibles from cephalopods; and exoskeletons from crustaceans. Prey items were identified with the aid of reference collections at the Duke University Marine Laboratory, the University of North Carolina’s Institute for Marine Sciences, and Mote Marine Laboratory. Published guides used to identify prey included Bigelow and Schroeder (1953), Chao (1978), Brouder (1979), Clarke (1986), Harkonen (1986), Robins etal. (1986), and Murdy etal. (1997). The number

URIAN,K. W., A. A. HOHNANDL. J. HANSEN.1999. Status of the Photo-identification catalog of coastal bottlenose dolphins of the western North Atlantic: Report of a workshop of catalog contributors. NOAA Technical Memorandum NMFS-SEFSC-425. (Available from the National Oceanic and Atmospheric Administration-Beaufort Laboratory, 101 Pivers Island Road, Beaufort, North Carolina 28516.) 5 30 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3, 2004 of either upper or lower mandibles (which ever was more abundant) from each species was used to determine the number of squid present. The abundance of each fish species in a stomach was determined by summing the number of intact fish and half the number of free otoliths. Atlantic menhaden (Brevoortia tyrannus) possess delicate otoliths, but they have high rates of parasitism, up to 46%, by the isopod Olencira praegustator (Kroger and Guthrie 1972, Lindsay and Moran 1976). During trawl surveys in North Carolina’s Neuse River estuary, 0. praegtlstator was found to parasitize only menhaden and no more than one isopod was found in each fish (Eby4; D. Gannon, unpublished data). The isopod’s chitonous exoskeleton is resistant to digestion, making it a good indicator of menhaden in the diet. Therefore, the minimum number of menhaden in each dolphin stomach was determined by either half the number of menhaden otoliths or by the number of isopods, which ever was greater. Relative importance of prey in the diet of bottlenose dolphins was determined by three methods: (1) frequency of occurrence, (2) proportion of numerical abundance, and (3)proportion of reconstructed mass. Frequency of occurrence is the proportion of dolphin stomachs containing a particular food type. Proportion of numerical abundance is the number of individuals of a prey species recovered from a particular stomach, divided by the total number of all prey from that stomach, averaged across all stomachs. Proportion of reconstructed mass is the sum of the masses of individuals of a prey species recovered from a particular stomach, divided by the total mass of all prey from that stomach, averaged across all stomachs. Wet weights of individual prey prior to ingestion were estimated from their lengths. We determined the sizes of prey by measuring intact organisms and by regressing the lengths of skeletal parts on body length for well-digested prey. Standard lengths were used for fish and mantle lengths were used for cephalopods. Standard lengths of partially digested fish were estimated from the lengths of sagittal otoliths. Squid mantle lengths were estimated from the lower rostra1 lengths of their mandibles (Clarke 1986). Otoliths were scored on a scale from 0 (undamaged otoliths retrieved from skulls) to 5 (severely degraded, free otoliths) following the methods of Recchia and Read (1989). Including severely eroded otoliths in analyses of ptey size can bias results negatively (da Silva and Neilson 1985, Jobling and Breiby 1986, Recchia and Read 1989). However, the ratio of surface area to volume affects the time required to digest a food item (Windell 1967), meaning that for a particular prey species, large individuals take longer to digest than do small ones. Therefore, it may be possible to over- estimate mean prey size by only including otoliths retrieved from intact skulls. To minimize these biases, we used otoliths categorized as 0, 1, and 2 to estimate sizes of prey. All intact prey and up to 30 undamaged otoliths of each species were measured from each stomach. Potential biases in selecting otoliths for measurement were minimized by the following protocol: (1) one otolith from each severed head was measured; (2) if a prey species was represented by fewer than 60 otoliths categorized as 0-2, half of those undamaged otoliths were randomly selected and measured; and (3) if a stomach contained more than 60 undamaged otoliths from one prey species, 30 were randomly selected and measured. For calculating the proportion of reconstructed mass, the lengths of damaged otoliths were estimated from the average lengths of undamaged otoliths contained in the same stomach. If all the otoliths of a particular prey species in a stomach were eroded, the sizes of these fish were

* Personal communication from Lisa Eby, Wildlife Biology Program, The University of Montana, Missoula, MT 69812, June 2003. GANNON AND WAPLES BOTTLENOSE WLPHIN DIET 531 estimated by taking the average size of that species eaten by other dolphins. Equations used to calculate standard length and weight of fish were obtained from Barros (1993) and Barros and Wells (1998). Equations for estimating the dorsal mantle length and wet weight of the squid Loligo sp. were those given by Gannon et al. (1997) and Lange and Johnson (1981) for L. pealei. Length-weight regressions were not available for all prey species. Therefore, analyses of reconstructed mass included only the seven most numerous prey; the combined masses of these seven species summed to 100%.

Bottlenose Dolphin Diet: Variation Between Habitats To investigate potential dietary differences between habitats, we matched each dolphin in our estuarine sample (n = 24) to one from the ocean sample according to location, season, sex, and length. Locations of strandings inside the estuaries were matched to those on ocean beaches according to latitude. The mean difference in latitude for each pair was 0.12‘. We defined the seasons as: winter = December- February; spring = March-May; summer = June-August; and fall = September- November. For each sex, dolphins were categorized as “juvenile” or “adult” (ie., sexually mature) by body length. Mead and Potter (1990) estimated mean length at sexual maturity to be 233.5 cm for females that stranded in an area that overlapped our study area. Working on Florida’s Gulf of Mexico coast, Wells et al. (1987) found that sexual maturity is reached at 230 cm and 245 cm for females and males, respectively. Since Wells et al. (1987) had data on both females and males, and their data on female maturation were similar to that of Mead and Potter (1990), we considered females to reach sexual maturity at 230 cm and males to mature at 245 cm, standard length. But it should be noted that Mead and Potter (1990) compared the age/length curve for bottlenose dolphins of the central Atlantic coast of the U.S. to that of animals from the Gulf of Mexico and found that the dolphins from the central Atlantic attained a higher asymptotic length (approximately 250 0s. 230 cm, both sexes combined).

Bottlenose Dolphin Diet: Seasonal Variation We explored seasonal variations in species composition and prey size among dolphins that died in the ocean. Due to the small sample size, this analysis could not be performed on the sample of dolphins obtained in the estuaries. Seasons were defined as above.

Bottlenose Dolphin Diet: Demographic Variation Among the sample of dolphins obtained from the ocean, we investigated whether different demographic groups tended to eat different species or whether there were any differences among demographic groups regarding the sizes of prey that they ate. The life history stages examined included: juvenile female (5 230 cm and having no visible signs of milk in the stomach), adult female (>230 cm), juvenile male (5 245 cm and having no signs of milk), and adult male (>245 cm; Wells et al. 1987). 532 MARINE MAMMAL SCIENCE. VOL. 20. NO. 3, 2004

Statistical Analysis We used Spearman’s rank correlation coefficient to assess differences in proportions of numerical abundance between samples of dolphins that died inside estuaries and those that died in the ocean, following the methods of Fritz (1974). Prey that were equally rare in both samples would exaggerate the dietary similarities between the groups. Therefore, only prey that accounted for 2 2% of numerical abundance in at least one of the samples were included in the analysis. To investigate differences in the proportional contributions of individual prey species associated with season and with demography, we used Kruskal-Wallis tests. Differences in the sizes of prey eaten by dolphins in each sample were tested with either Mann- Whitney U tests or Kruskal-Wallis tests, depending on the number of samples being compared. For comparisons of prey length only food items represented by otoliths graded as 0, 1, or 2 were used; otoliths that were eroded more severely were excluded. The individual dolphin was the unit of analysis, meaning that the average lengths of each species consumed by each dolphin were used in these analyses. To facilitate interpretation of feeding data, we investigated whether there were any differences in the sizes of the dolphins between the estuarine and oceanic samples and among the samples from the four seasons using the Mann-Whitney and Kruskal Wallis tests, respectively. Standard deviation is given as a measure of variability about the mean and is presented using the convention x t SD. All statistics were calculated using SigmaStat version 2.03.

RESULTS We examined the stomach contents of 186 bottlenose dolphins that died in the estuarine and nearshore ocean waters of North Carolina (Fig. 1). Based on the presence of “offshore” prey (e.g., Ommastrephid and Histioteuthid squids) and parasites, six dolphins were categorized as being the offshore ecotype and were excluded from further analyses. The 17 dolphins with stock identities known from sighting histories and location of death were classified correctly by the combination of prey and parasite assemblages. Of the 180 stomachs from coastal dolphins, 146 contained solid food, seven contained only milk, and 27 were empty (Appendix 1). The largest juvenile whose stomach contained only milk and had no evidence of solid food (prey remains or stomach parasites) was 164 cm in length. The smallest dolphin with solid food (and the stomach parasite Braunina sp.) was 146 cm. Of the dolphins that had remains of solid food, 71 (49%) bore evidence that interactions with humans caused death, such as entanglement in monofilament gill net and mutilation; 22 (15 %) had no evidence of human interaction, and cause of death was not assessed in 53 (36%) cases. At least 21 families and 31 species of prey were found in the diet of the dolphins (Table 1). Fishes from the family Sciaenidae dominated the diet, appearing in 95% of dolphin stomachs, and accounting for 73% of all food items eaten. Weakfish (Cynoscion regalis), croaker, and spot were the most important prey, followed distantly by inshore squid (Loligo sp.) and striped anchovy (Anchoa hepsetus). Length- frequency distributions of weakfish, spot, and croaker are shown in Figure 2. The weakfish eaten tended to be larger (mean = 244+.60 mm) than the other prey (croaker: mean = 157 t 35; spot: mean = 131 ? 31), which is reflected by this species’ reconstructed mass values being substantially higher than its numerical abundance values. GANNON AND WAPLES: BOTTLENOSE DOLPHIN DIET 533

Figure 1. Stranding locations of bottlenose dolphins (Tursiops truncutus) that were included in analyses of food habits. Triangles indicate carcasses recovered from the ocean and circles indicate carcasses recovered from the estuary.

Bottlenose Dolphin Diet: Variation Between Habitats There was no significant difference between the estuarine and oceanic samples regarding the sizes of the dolphins (U = 352.5, P = 0.43). Eight prey species accounted for >. 2% of numerical abundance in either the “ocean” or “estuary” sample: croaker, weakfish, spot, inshore squid, striped anchovy, shrimp eel (Opbich- thus gomesi), menhaden, and black drum (Pogonias cromis; Fig. 3). Croaker and spot dominated the stomach contents of dolphins stranded inside the estuaries (Fig. 3A). Croaker accounted for 51% of numerical abundance (92% by frequency of occurrence and 63% by proportion of mass) and spot contributed 26% (75% by frequency of occurrence and 19% by proportion of mass). Dolphins that stranded along ocean beaches had large amounts of weakfish, croaker, spot, inshore squid, and striped anchovy in their stomachs (Fig. 3B). The Spearman rank correlation coefficient (r,) for numerical abundance values of estuary and ocean dolphins was 0.419 (P = 0.213), indicating that there was no statistical relationship between the rank orders of prey in the diets of these two groups. The average sizes of weakfish, croaker, and spot eaten by dolphins in the ocean were larger than those eaten by dolphins in the estuaries. These differences were significant in the cases of weakfish and spot. The average standard length of weakfish eaten by dolphins in the ocean sample was 256 +- 56 mm, while that of weakfish eaten by dolphins in the estuary sample was 208 ? 57 mm (Mann-Whitney test: 5 34 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3, 2004

Table 1. Relative importance of prey measured by (1) frequency of occurrence, (2) proportion of numerical abundance and (3) proportion of reconstructed mass, and proportion of otoliths recovered from skulls (Grade = 0) for prey of “oceanic” and “estuarine” coastal Twsiops truncatus from North Carolina (n = 146).

Frequency Numerical Mass Grade-0 Prey (%I (%) (%) Otoliths (%) CHORDATA 98 96 Sciaenidae 95 73 Weakfish (Cynoscion regalis) 65 24 Croaker (Micropogonids undulatus) 47 22 Spot (hiortomus xanthurus) 54 20 Silver perch (Bairdiella chrysoura) 29 3 Kingfish sp. (Menticirrhus sp.) 13 1 Black drum (Pogonias cromis) 12 1 Red drum (Sciaenops odatus) G 1 Star drum (Stellif.. lanceolatus) 3 <1 Unidentified fish 31 7 Unidentified fish spp. 31 7 Engraulidae 24 6 Striped anchovy (Anchoa hepsetus) 24 6 Clupeidae 19 2 Menhaden (Brevoortia tyrannus) 19 2 Sparidae 19 2 Pinfish (Lagodon rhomboides) 8 1 Sparidae spp. 12 Spottail pinfish (Diplodus bolbrooki) 1 <1 Pigfish (Ortbopristis chrysoptera) 17 1 Bothidae 15 1 Flounder (Parafichthys sp.) 8 <1 Whiff (Citharichthys sp.) 12 <1 Gadidae 8 1 Hake (Urophycis @.) 8 1 Ophichthidae 4 1 Shrimp eel (Opbichthm gomesi) 4 1 Mugilidae 3 <1 Mullet (Mugif cephafus) 3 (1 Synodontidae 3 <1 Lizardfish (Synodus foetens) 3 <1 Percichthyidae 2 <1 Striped bass (Morone saxatilis) 2 <1 Carangidae 2

Table 1. Continued.

Frequency Numerical Mass Grade-0 Prey (%I (%I (%) Otoliths (%) Order Lamniformes 1 Unidentified shark 1 MOLLUSCA 30 Loliginidae 30 Inshore squid (Loligo sp.) 26 Brief squid (Loligunczlla brevis) 4 CRUSTACEA 8 Order Stomatopoda 1 Mantis shrimp (4 families) 1 Penaeidae 6 Shrimp (species?) 6 Alpheidae 1 Alpheus sp. 1 Portunidae 1 Blue crab (CallinectesJabidas) 1

a - = no data.

U = 186.5, P = 0.007). The average spot eaten in the estuary was 118 2 34 mm, while the average spot consumed in the ocean was 141 If: 25 mm (U = 206.0, P = 0.001). For croaker, the average size in the ocean sample was 165+38 mm whereas that of the estuary sample was 144 If: 22 mm (U = 194.0, P = 0.062). Stomachs of dolphins in the estuary sample contained significantly more prey items (115 ? 143) than those from the ocean sample (48 t 67; U = 876.0, P = 0.002).

Bottlenose Dolphin Diet: Seusonal Vuriution For the dolphins that stranded on ocean beaches, there was no difference in dolphin size with regard to the seasons in which stranding occurred (Kruskal-Wallis test: H = 0.42, df = 3, P = 0.94). However, there was considerable variation in the diet associated with season (Fig. 4). For example, the numerical proportion of croaker varied by an order of magnitude across seasons, reaching a high of 61% in summer and a low of 6% in winter (H= 23.1, df= 3, P < 0.01). The contributions of spot were consistent at about 15% from winter to summer, but increased to 35% in fall (H = 14.25, df = 3, P < 0.01). Weakfish were extremely important during winter (47%) and spring (34%), but dropped in importance in summer (8%)and fall (6%; H=21.19,df=3,P < 0.01).Inshoresquidcomprised 8%-10% ofthediet for most of the year, but then dropped to just 1% in summer. However, differences in the numerical proportions of inshore squid across seasons were not significant (H = 0.78, df= 3, P = 0.85 5). Despite the large variations in diet composition throughout the year, there were no differences in sizes of prey associated with season (weakfish: H=5.94,df=3, P=O.l14;spot: H=4.19,df=3,P=0.242;croaker: H=2.09, df = 3, P = 0.554; Table 2). 5 36 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3, 2004

Croaker (n=599) i:_0.06

0.04 0.02 0

Spot (113630) 0.160.14 1 0.12 0.1 0.08 0.06 0.04 0.02 0

0.18

0.16 - Weakfish (n=594) 0.14 -

0.12 -

0.1 - 0.08 - 0.06 0.04 0.02 0

Figwe 2. Length-frequency distributions of croaker, spot, and weakfish eaten by coastal bottlenose dolphins in North Carolina waters. Solid bars indicate length estimates made from otoliths graded as 0 (retrieved from skulls) and open bars are from otoliths graded as 1 (free in the stomach, undamaged) and 2 (free in the stomach, slightly damaged). GANNON AND WAPLES: BOTTLENOSE DOLPHIN DIET 537

Figwe 3. Numerical abundance 1%) of prey from stomach contents of coastal bottlenose dolphins that died in the (a) estuarine and (b) ocean waters of North Carolina. Each dolphin in the estuary sample is matched with one in the ocean sample by season, demographic group, and latitude.

Bottlenose Dolphin Diet: Demographic Variation Croaker comprised a greater percentage of the diet for males than for females, and mature dolphins ate more croaker than did juveniles (Fig. 5). The differences in the numerical proportions of croaker eaten by each demographic group were significant (H = 8.82, df= 3, P = 0.032). Juvenile dolphins ate proportionately more spot than did adults, whereas adults ate more weakfish. However, among the four demographic groups investigated, there were no significant differences in the numerical proportions of spot, weakfish, or inshore squid eaten (spot: H = 6.88, df = 3, P = 0.076; weakfish: H = 2.22, df = 3, P = 0.528; inshore squid: H = 1.99, df = 3, P = 0.57 5). There were no significant differences among the four dolphin demographic groups regarding the sizes of prey (Table 3). As with the investigation of the effects 538 MARINE MAMMAL SCIENCE, VOL. 20. NO. 3, 2004

Figure 4. Numerical abundance (%) of prey from stomach contents of oceanic coastal bottlenose dolphins by season. of season on prey size, sample sizes of some prey eaten by some demographic categories of dolphins were small.

DISCUSSION Although coastal bottlenose dolphins from North Carolina ate a wide variety of prey, their diet was composed primarily of soniferous, demersal species from the family Sciaenidae. Three species-croaker, weakfish, and spot-accounted for 66% of the diet by proportion of numerical abundance. There were significant variations in the diet associated with habitat (ocean M. estuary), season, and dolphin demography, which have not been investigated previously. These variations in the foods eaten may have resulted from spatial or temporal variations in prey availability, from ontogenetic changes in feeding preference, or from differences in habitat selection. It seems likely that demographic differences in diets among dolphins that died in the ocean resulted primarily from differences in feeding preferences, in feeding abilities, or in habitat selection. Dietary differences among seasons and between habitats may have also reflected differences in prey availability. For example, weakfish was more prominent in the diets of mature dolphins than in those of juveniles, perhaps reflecting the difficulty of capturing this swift prey. Inshore squid was far more important to mature females than it was to the other demographic groups, which may have resulted from mothers with calves having different habitat preferences from other demographic groups or it could have resulted from reproductive females GANNON AND WAPLES: BOTTLENOSE DOLPHIN DIET 539

Table 2. Mean and standard deviations of standard lengths (mm) of weakfish, croaker, and spot eaten by oceanic coastal bottlenose dolphins off North Carolina during all four seasons. Sample size (n) refers to the number of dolphin stomachs with measurable prey.

Weakfish n Croaker n spot n Winter 274 2 55 23 158 f 0 2 130 2 14 4 Spring 247 * 55 29 171 ? 39 8 131 f 24 18 Summer 214 2 54 6 134 ? 15 6 138 2 21 3 Fall 258 2 54 8 166 ? 38 12 152 2 30 17

broadening their diet to meet the increased energy demands of lactation. Similar patterns have been found in other delphinids. Robertson and Chivers (1997) noted in spotted dolphins (Stenella attenaata), that the diet of lactating females contained higher proportions of squids than did that of pregnant females (but see Bernard and Hohn 1989). Dietary differences between dolphins that died in estuaries and those that died in the ocean were consistent with the habitat partitioning hypothesis, whereby some members of the population are principally estuarine and others are primarily oceanic. The diet of dolphins in the estuaries was dominated by Atlantic croaker and spot, while the diet of the dolphins that died in the ocean was dominated by weakfish. Additionally, the prey consumed by dolphins in the ocean tended to be larger than those eaten by dolphins in the estuaries. The differences between the two habitats regarding prey composition and prey size were not likely to have been caused by sampling bias, since we controlled for size, sex, season, and location. We could not determine whether any of these differences in diet resulted from differences in prey availability between the two habitats or from differences in prey selection by the dolphins in the two habitats. Fisheries data are collected using different techniques in the two habitats and, therefore, are inappropriate for statistical comparisons. However, catches in demersal trawl surveys of the Neuse River estuary were similar to the diets of dolphins that died in the estuaries; croaker and spot were the two most abundant species and young-of-the-year fish represented the greatest proportion of the catch (Eby and Crowder 2002, Gannon 2003). Juveniles of all three major prey-weakfish, croaker, and spot-use estuaries as nursery habitat (Chao and Musick 1977, Currin et al. 1984), and therefore the average sizes of individuals from these species may be smaller in the estuary than in the ocean. Coastal oceans tend to have higher species richness relative to estuaries

Table 3. Mean and standard deviations of standard lengths (mm) of weakfish, croaker, and spot eaten by four demographic groups of oceanic coastal botrlenose dolphins off North Carolina. Sample size (n) refers to the number of dolphin stomachs with measurable prey.

Weakfish n Croaker n spot n Female <230 cm 221 2 73 9 151 ? 40 5 122 2 23 7 Female 2230 cm 269 2 48 20 184 2 19 4 158 2 25 7 Male <245 cm 253 t 57 22 150 2 30 14 138 2 24 20 Male 2245 cm 262 2 56 12 189 t 39 5 154 2 36 5 540 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3, 2004

Figure 5. Numerical abundance (%) of prey from stomach contents of oceanic coastal bottlenose dolphins by demographic group.

(Remane and Schlieper 1971), and this difference in diversity was reflected in the diets of our two dolphin samples. Our findings that sciaenids dominate the diet of coastal bottlenose dolphins agree well with those of Mead and Potter (1990) and Barros (1993). With a sample of stranded bottlenose dolphins from North Carolina, Virginia, and Maryland, Mead and Potter (1990) found weakfish, spot, and croaker to be the most frequently occurring prey. The largest differences were in the occurrences of engraulids, sparids, haemulids, and gadids (24%, 19%, 1796, and 8% in our sample, respectively). Mead and Potter found engraulids (8%), haemulids (2%), and sparids (0%) to be much less common, and gadids (16%) to be more common. Barros’s (1993) sample from dolphins stranded on ocean beaches in northeast Florida was very similar to our ocean sample. However, Barros’s sample from the Indian River Lagoon in northeast Florida contained relatively few weakfish but did include large numbers of spotted seatrout (Cynoscion nebulosus), silver perch, oyster toadfish (Opsanus tau), and striped mullet (Mugil cepbalus). Working with stranded specimens from the area of Sarasota Bay, Florida, Barros and Wells (1998) found relatively few sciaenids in the diet; the three most abundant prey were pinfish (Lagodon rbomboides), striped mullet, and pigfish (Orthopristis cbysoptera). The paucity of sciaenids in the diet of Sarasota Bay dolphins may reflect lower relative abundance of these fishes in the subtropical fish community of southwest Florida (Wessel and Winner 2003). None of these other studies were able to investigate differences in the diet associated with season or demography. GANNON AND WAPLES: BOTTLENOSE DOLPHIN DIET 541

Soniferous fishes account for 75% of the total number of prey in Table 1 (Sciaenids, Sparids, Haemulids, Carangids, and Batrachoidids; see Fish and Mowbray 1970). The Sciaenidae, in particular, is one of the most prolific sound- producing families of fish. The dominance of soniferous species in the diet is consistent with Barros’s hypothesis that coastal bottlenose dolphins use passive listening to locate noise-producing prey (Barros and Ode11 1990, Barros 1993, Barros and Wells 1998). Listening is an important mode of prey detection for a wide variety of taxa including owls (Bye et al. 1992) and bats (Marimuthu and Neuweiler 1987, Bailey and Haythornthwaite 1998). There is also evidence that odontocetes hunt by passive listening. Mammal-eating killer whales (Orcinzls orcu) appear to rely heavily on passive listening for prey detection. Whereas fish-eating killer whales use echolocation extensively, their mammal-eating conspecifics echolocate sparingly (Barrett-Lennard et ul. 1996). Barrett-Lennard and his colleagues attributed the differences in hunting strategies of the two forms to differences in the ecological costs of echolocation incurred by each form. Pinnipeds and cetaceans can hear the killer whales’ echolocation signals but salmonid fishes cannot. Therefore, when mammal-eating whales echolocate, they reveal their presence to their prey. Other coastal delphinids may also use passive listening to locate chorusing sciaenids. Pilleri et al. (1982) noted a high degree of co-occurrence between the Indian humpback dolphin (Soma pltlmbea) and chorusing aggregations of Johitls belangerii. De Olivera Santos et al. (2002) found that 92% of the teleosts eaten by marine tucuxi dolphins (Sotulia jluviatilis) in Brazilian waters were sciaenids, leading these authors to hypothesize that tucuxi locate prey via passive listening. If piscivores use acoustic cues to locate prey, then sound production could be a very costly activity for fishes, and the risks of calling should be traded off with the benefits of this behavior. Sound production in sciaenids is often associated with spawning (Fish and Mowbray 1970, Connaughton and Taylor 1995, Luczkovich et al. 1999). Calling may be a way for males to attract mates or may play a role in synchronizing the release of gametes. Therefore, the potential costs of remaining silent may be reduced reproductive success. Given that both the risks and benefits of calling appear to be high for fish, one might expect them to be under intense selection pressure to be able to detect their predators and to modify their calling behavior when predators are present. Indeed, Luczkovich et al. (2000) documented a reduction in the received amplitude of silver perch spawning choruses in response to playbacks of recorded sounds from bottlenose dolphins. Despite data indicating that many vertebrate taxa detect prey by passive acoustics and that the prey eaten by coastal bottlenose dolphins in North Carolina produce sound, it is still not clear how the dolphins in this study could have used passive listening to detect their prey. The spatiotemporal pattern in consumption of Sciaenid species did not correspond with the pattern of their spawning, which is when they are thought to produce sound most frequently (Fish and Mowbray 1970, Connaughton and Taylor 1995, Luczkovich et al. 1999). For example, Atlantic croaker spawn in the ocean during winter (Hildebrand and Cable 1930, Chao and Musick 1977, Warlen and Burke 1990), but they were eaten most often by dolphins inside the estuaries and by dolphins in the ocean during summer (Fig. 3, 4). Weakfish, on the other hand, spawn in the estuaries during May and June (Connaughton and Taylor 1995, Luczkovich et al. 1999), but they were eaten most commonly in the ocean during winter. These data suggest two possibilities: (1) that bottlenose dolphins do not rely on passive listening to any great extent for detecting prey, or (2) that these fishes have a larger repertoire of sounds than is 542 MARINE MAMMAL SCIENCE, VOL. 20. NO. 3, 2004 currently believed, including sounds that are not associated with spawning. To understand the nature of the interactions that take place between coastal bottlenose dolphins and their prey, and to gain better insights into the ecology of sound production by fishes, the passive listening hypothesis needs to be tested experimentally, and more rigorous behavioral studies of sound production by sciaenids need to be conducted.

ACKNOWLEDGMENTS Sue Barco, Tara Cox, Ari Friedlander, Heather Koopman, Rachel Lopicollo, Patrick Martone, Bill Mclellan, Ann Pabst, Jeremy Rusin, Karen Sayles, Vicky Thayer, Katie Touhey, Andrew Westgate, and the Southeastern Regional Stranding Network, administered by the Beaufort Laboratory of the National Marine Fisheries Service, collected dolphin stomachs. NClio Barros, Bill Kirby-Smith, Charles Manooch, and Frank Schwartz helped identify prey. Kim Urian provided photo-identification data. Andy Read, NClio Barros, Larry Crowder, Bill Kirby-Smith, and Jessica Maher reviewed early drafts. Two anonymous reviewers helped improve the final manuscript. This work was funded by a grant from the U.S. Environmental Protection Agency to L. Crowder and A. Read (grant no. R261000-01- 0). D.P.G. was also supported by a Duke Marine Laboratory Graduate Fellowship.

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Appendix 1. Numbers of Tursiops truncatw stomachs examined for analyses of food habits.

Total number of dolphin stomachs examined 186 Stomachs from dolphins recovered in the ocean 154 Empty “ocean” stomachs 19 Ocean stomachs containing only milk 7 Ocean stomachs containing solid food 128 Stomachs from offshore dolphins containing food 6 Stomachs from “coastal ocean” dolphins containing food 122 Females <230 cm with food 24 Females 2230 cm with food 29 Males <245 cm with food 42 Males 2245 cm with food 18 Sex unknown 9 Winter 33 Spring 51 Summer 7 Fall 27 Date unknown 4 Stomachs from dolphins recovered in estuaries 32 Empty “estuarine” stomachs 8 Estuarine stomachs containing only milk 0 Estuarine stomachs containing solid food 24 Females <230 cm with food 4 Females 2230 cm with food 3 Males (245 cm with food 9 Males 2245 cm with food 5 Sex unknown 3 Winter 4 Spring 10 Summer 6 Fall 4